Overexpression of microRNA319 impacts leaf morphogenesis and leads to enhanced cold tolerance in rice (Oryza sativaL.)

Plant, Cell and Environment

Volumn 36, Issue 12, 2013, Pages 2207-2218

  Yang, Chunhua ^a   Li, Dayong ^a   Mao, Donghai ^b   Liu, Xue ^a   Ji, Chengjun ^c   Li, Xiaobing ^a   Zhao, Xianfeng ^a   Cheng, Zhukuan ^a   Chen, Caiyan ^b   Zhu, Lihuang ^a  

^a INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

Leaf development; miR319; TCP genes

Indexed keywords

COLD TOLERANCE; DICOTYLEDON; GENE EXPRESSION; LEAF; MORPHOGENESIS; RICE; RNA; SPECIES DIVERSITY;

DICOTYLEDONEAE; LILIOPSIDA; ORYZA; OSA;

MICRORNA;

ADAPTATION; ARTICLE; COLD; DOWN REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; LEAF DEVELOPMENT; METABOLISM; MIR319; MOLECULAR GENETICS; MORPHOGENESIS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT LEAF; RICE; TCP GENES; TRANSGENIC PLANT;

LEAF DEVELOPMENT; MIR319; TCP GENES;

ADAPTATION, PHYSIOLOGICAL; BASE SEQUENCE; COLD TEMPERATURE; DOWN-REGULATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MICRORNAS; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; ORYZA SATIVA; PHENOTYPE; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; STRESS, PHYSIOLOGICAL;

EID: 84886395963     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.12130     Document Type: Article

References (61)

1. Ahamed A., Murai-Hatano M., Ishikawa-Sakurai J., Hayashi H., Kawamura Y. & Uemura M. (2012) Cold stress-induced acclimation in rice is mediated by root-specific aquaporins. Plant and Cell Physiology 53, 1445-1456.
2. Andaya V.C. & Mackill D.J. (2003) Mapping of QTLs associated with cold tolerance during the vegetative stage in rice. Journal of Experimental Botany 54, 2579-2585.
3. Anderson M.D., Prasad T.K., Martin B.A. & Stewart C.R. (1994) Differential gene expression in chilling-acclimated maize seedlings and evidence for the involvement of abscisic acid in chilling tolerance. Plant Physiology 105, 331-339.
4. Axtell M.J. & Bowman J.L. (2008) Evolution of plant microRNAs and their targets. Trends in Plant Science 13, 343-349.
5. Bartel D.P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297.
6. Bartel D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
7. Ben-Gera H. & Ori N. (2012) Auxin and LANCEOLATE affect leaf shape in tomato via different developmental processes. Plant Signaling & Behavior 7, 1255-1257.
8. Chen X. (2008) MicroRNA metabolism in plants. Current Topics in Microbiology and Immunology 320, 117-136.
9. Chinnusamy V., Zhu J. & Zhu J.K. (2007) Cold stress regulation of gene expression in plants. Trends in Plant Science 12, 444-451.
10. Cuperus J.T., Fahlgren N. & Carrington J.C. (2011) Evolution and functional diversification of MIRNA genes. The Plant Cell 23, 431-442.
11. Dubouzet J.G., Sakuma Y., Ito Y., Kasuga M., Dubouzet E.G., Miura S., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. The Plant Journal 33, 751-763.
12. Fattash I., Voss B., Reski R., Hess W.R. & Frank W. (2007) Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biology 7, 13 (http://www.biomedcentral.com/1471-2229/7/13/).
13. Griffiths-Jones S., Saini H.K., van Dongen S. & Enright A.J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Research 36, D154-D158.
14. Guo H.S., Xie Q., Fei J.F. & Chua N.H. (2005) MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. The Plant Cell 17, 1376-1386.
15. Hiei Y., Ohta S., Komari T. & Kumashiro T. (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271-282.
16. Ito Y., Katsura K., Maruyama K., Taji T., Kobayashi M., Seki M., Shinozaki K. & Yamaguchi-Shinozaki K. (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant and Cell Physiology 47, 141-153.
17. Jin Y., Luo Q., Tong H., etal. (2011) An AT-hook gene is required for palea formation and floral organ number control in rice. Developmental Biology 359, 277-288.
18. Jung H.J. & Kang H. (2007) Expression and functional analyses of microRNA417 in Arabidopsis thaliana under stress conditions. Plant Physiology and Biochemistry 45, 805-811.
19. Kasschau K.D., Xie Z., Allen E., Llave C., Chapman E.J., Krizan K.A. & Carrington J.C. (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Developmental Cell 4, 205-217.
20. Khraiwesh B., Zhu J.K. & Zhu J. (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochimica et Biophysica Acta 1819, 137-148.
21. Kikuchi S., Satoh K., Nagata T., etal. (2003) Collection, mapping, and annotation of over 28, 000 cDNA clones from japonica rice. Science 301, 376-379.
22. Koyama T., Furutani M., Tasaka M. & Ohme-Takagi M. (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary-specific genes in Arabidopsis. The Plant Cell 19, 473-484.
23. Koyama T., Mitsuda N., Seki M., Shinozaki K. & Ohme-Takagi M. (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. The Plant Cell 22, 3574-3588.
24. Larcher W. (1995) Plants under stress. In Physiological Plant Ecology (ed. W. Larcher), pp. 321-448. Springer-Verlag, Berlin.
25. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H. & Kim V.N. (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal 23, 4051-4060.
26. Li Y., Zhang Q., Zhang J., Wu L., Qi Y. & Zhou J.M. (2010) Identification of microRNAs involved in pathogen-associated molecular pattern-triggered plant innate immunity. Plant Physiology 152, 2222-2231.
27. Liu H.H., Tian X., Li Y.J., Wu C.A. & Zheng C.C. (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14, 836-843.
28. Lu S., Sun Y.H., Amerson H. & Chiang V.L. (2007) MicroRNAs in loblolly pine (Pinus taeda L.) and their association with fusiform rust gall development. The Plant Journal 51, 1077-1098.
29. Lv D.K., Bai X., Li Y., Ding X.D., Ge Y., Cai H., Ji W., Wu N. & Zhu Y.M. (2010) Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene 459, 39-47.
30. Mao D. & Chen C. (2012) Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS ONE 7, e47275.
31. Nag A., King S. & Jack T. (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 106, 22534-22539.
32. Nath U., Crawford B.C., Carpenter R. & Coen E. (2003) Genetic control of surface curvature. Science 299, 1404-1407.
33. Navarro L., Dunoyer P., Jay F., Arnold B., Dharmasiri N., Estelle M., Voinnet O. & Jones J.D. (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312, 436-439.
34. Nelson T. & Dengler N. (1997) Leaf vascular pattern formation. The Plant Cell 9, 1121-1135.
35. Ori N., Cohen A.R., Etzioni A., etal. (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nature Genetics 39, 787-791.
36. Palatnik J.F., Allen E., Wu X., Schommer C., Schwab R., Carrington J.C. & Weigel D. (2003) Control of leaf morphogenesis by microRNAs. Nature 425, 257-263.
37. Palatnik J.F., Wollmann H., Schommer C., etal. (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Developmental Cell 13, 115-125.
38. Pandey S.P. & Baldwin I.T. (2007) RNA-directed RNA polymerase 1 (RdR1) mediates the resistance of Nicotiana attenuata to herbivore attack in nature. The Plant Journal 50, 40-53.
39. Poethig R.S. (2009) Small RNAs and developmental timing in plants. Current Opinion in Genetics & Development 19, 374-378.
40. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B. & Bartel D.P. (2002) MicroRNAs in plants. Genes & Development 16, 1616-1626.
41. Satoh K., Doi K., Nagata T., etal. (2007) Gene organization in rice revealed by full-length cDNA mapping and gene expression analysis through microarray. PLoS One 2, e1235.
42. Scarpella E. & Meijer A.H. (2004) Pattern formation in the vascular system of monocot and dicot plant species. New Phytologist 55, 209-242.
43. Scarpella E., Rueb S. & Meijer A.H. (2003) The RADICLELESS1 gene is required for vascular pattern formation in rice. Development 130, 645-658.
44. Schommer C., Palatnik J.F., Aggarwal P., Chetelat A., Cubas P., Farmer E.E., Nath U. & Weigel D. (2008) Control of jasmonate biosynthesis and senescence by miR319 targets. PLoS Biology 6, e230.
45. Schommer C., Bresso E.G., Spinelli S.V. & Palatnik J.F. (2012) Role of micro-RNA miR319 in plant development. In MicroRNAs in Plant Development and Stress Responses, Signaling and Communication in Plants, Vol. 15 (ed. R. Sunkar), pp. 29-47. Springer-Verlag, Berlin, Heidelberg.
46. Schwab R., Palatnik J.F., Riester M., Schommer C., Schmid M. & Weigel D. (2005) Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8, 517-527.
47. Shleizer-Burko S., Burko Y., Ben-Herzel O. & Ori N. (2011) Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development 138, 695-704.
48. Sunkar R. & Zhu J.K. (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. The Plant Cell 16, 2001-2019.
49. Talmor-Neiman M., Stav R., Frank W., Voss B. & Arazi T. (2006) Novel micro-RNAs and intermediates of micro-RNA biogenesis from moss. The Plant Journal 47, 25-37.
50. Thiebaut F., Rojas C.A., Almeida K.L., Grativol C., Domiciano G.C., Lamb C.R., Engler Jde A., Hemerly A.S. & Ferreira P.C. (2012) Regulation of miR319 during cold stress in sugarcane. Plant, Cell & Environment 35, 502-512.
51. Thomashow M.F. (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571-599.
52. Tsukaya H. (2006) Mechanism of leaf-shape determination. Annual Review of Plant Biology 57, 477-496.
53. Voinnet O. (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687.
54. Wahid F., Shehzad A., Khan T. & Kim Y.Y. (2010) MicroRNAs: synthesis, mechanism, function, and recent clinical trials. Biochimica et Biophysica Acta 1803, 1231-1243.
55. Wang Z., Chen C., Xu Y.Y., Jiang R.X., Han Y., Xu Z. & Chong K. (2004) A practical vector for efficient knockdown of gene expression in rice (Oryza sativa L.). Plant Molecular Biology Reporter 22, 409-417.
56. Warthmann N., Das S., Lanz C. & Weigel D. (2008) Comparative analysis of the MIR319a microRNA locus in Arabidopsis and related Brassicaceae. Molecular Biology and Evolution 25, 892-902.
57. Weigel D., Ahn J.H., Blazquez M.A., etal. (2000) Activation tagging in Arabidopsis. Plant Physiology 122, 1003-1013.
58. Yanai O., Shani E., Russ D. & Ori N. (2011) Gibberellin partly mediates LANCEOLATE activity in tomato. The Plant Journal 68, 571-582.
59. Zhou L., Liu Y., Liu Z., Kong D., Duan M. & Luo L. (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany 61, 4157-4168.
60. Zhou M., Li D., Li Z., Hu Q., Yang C., Zhu L. & Luo H. (2013) Constitutive expression of a miR319 gene alters plant development and enhances salt and drought tolerance in transgenic creeping bentgrass. Plant Physiology 161, 1375-1391.
61. Zhu J.K. (2008) Reconstituting plant miRNA biogenesis. Proceedings of the National Academy of Sciences of the United States of America 105, 9851-9852.